Structural variation of a sex-linked region confers monoecy and implicates GATA15 as a master regulator of sex in Salix purpurea

Authors: HYDEN, BRENNAN - Cornell University; ZOU, JUNZHU - Cornell University; WILKERSON, DUSTIN - Cornell University; Carlson, Craig; ROBLES RIVIERA, AYIANA - Cornell University; DIFAZIO, STEPHEN - Cornell University; SMART, LAWRENCE - Cornell University

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/21/2023
Publication Date: 5/17/2023
Citation: Hyden, B., Zou, J., Wilkerson, D.G., Carlson, C.H., Robles Riviera, A., Difazio, S., Smart, L. 2023. Structural variation of a sex-linked region confers monoecy and implicates GATA15 as a master regulator of sex in Salix purpurea. New Phytologist. 238(6):2512-2523. https://doi.org/10.1111/nph.18853.
DOI: https://doi.org/10.1111/nph.18853

Interpretive Summary: Willows are diverse plants with uses in bioenergy, ornamental horticulture, and ecological restoration. Willows have separate male and female plants (dioecy), opposed to having male and female flowers on the same plant (monoecy), which is more common among seed producing plants. This presents several limitations for breeding, notably, by reducing the possible combinations and types of crosses. We identified a rare willow individual, having both male and female flowers on the same plant, and generated families using itself and other males or females as parents. Over three years, we characterized the proportion of male and female flowers of all family individuals, which were relatively stable across environments. The expression of individuals' sex (all male, all female, or both) served as the basis for developing new models of inheritance. By sequencing these families, we identified several genes associated with biomass growth, and importantly, the genetic basis of monoecy in willow, which was previously unknown. This research provides novel genetic resources to the willow research community and benefits a broad scientific audience by providing new knowledge about sex determination in flowering plants.

Technical Abstract: The Salicaceae are dioecious perennials that comprise several unique sex systems, and there is substantial interest in understanding the impacts of hybridization, speciation, and polyploidy on sex chromosome evolution. Here, a rare monoecious S. purpurea genotype, 94003, was self- and cross-pollinated to test existing sex determination hypotheses on segregating progeny. To delimit genomic regions associated with monoecious expression, the 94003 genome was assembled and DNA- and RNA-Seq of progeny inflorescences was performed. Based on linkage analysis and sequence alignments to dioecious and monoecious genomes, a 1.15 Mb sex-linked region on Chr15W was identified as absent in monecious plants. Inheritance of this structural variation is responsible for the loss of a male-suppressing function in what would otherwise be genetic females (Z/W), resulting in monoecy (Z/W^H or W/W^H), or lethality, if homozygous (W^H/W^H). Finally, we present a refined, two-gene sex determination model for S. purpurea, mediated by ARR17 and GATA15.